An atlas of active enhancers across human cell types and tissues

Robin Andersson, Claudia Gebhard, Irene Miguel-Escalada, Ilka Hoof, Jette Bornholdt, Mette Boyd, Yun Chen, Xiaobei Zhao, Christian Schmidl, Takahiro Suzuki, Evgenia Ntini, Erik Arner, Eivind Valen, Kang Li, Lucia Schwarzfischer, Dagmar Glatz, Johanna Raithel, Berit Lilje, Nicolas Rapin, Frederik Otzen Bagger, Mette Jørgensen, Peter Refsing Andersen, Nicolas Bertin, Owen Rackham, A. Maxwell Burroughs, J. Kenneth Baillie, Yuri Ishizu, Yuri Shimizu, Erina Furuhata, Shiori Maeda, Yutaka Negishi, Christopher J. Mungall, Terrence F. Meehan, Timo Lassmann, Masayoshi Itoh, Hideya Kawaji, Naoto Kondo, Jun Kawai, Andreas Lennartsson, Carsten O. Daub, Peter Heutink, David A. Hume, Torben Heick Jensen, Harukazu Suzuki, Yoshihide Hayashizaki, Ferenc Müller, Alistair R. R. Forrest (), Piero Carninci (), Michael Rehli () and Albin Sandelin ()
Additional contact information
Robin Andersson: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Claudia Gebhard: University Hospital Regensburg, Franz-Josef-Strauss-Allee 11, 93042 Regensburg, Germany
Irene Miguel-Escalada: School of Clinical and Experimental Medicine, College of Medical and Dental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
Ilka Hoof: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Jette Bornholdt: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Mette Boyd: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Yun Chen: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Xiaobei Zhao: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Christian Schmidl: University Hospital Regensburg, Franz-Josef-Strauss-Allee 11, 93042 Regensburg, Germany
Takahiro Suzuki: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Evgenia Ntini: Centre for mRNP Biogenesis and Metabolism, C.F. Møllers Alle 3, Building 1130, DK-8000 Aarhus, Denmark
Erik Arner: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Eivind Valen: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Kang Li: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Lucia Schwarzfischer: University Hospital Regensburg, Franz-Josef-Strauss-Allee 11, 93042 Regensburg, Germany
Dagmar Glatz: University Hospital Regensburg, Franz-Josef-Strauss-Allee 11, 93042 Regensburg, Germany
Johanna Raithel: University Hospital Regensburg, Franz-Josef-Strauss-Allee 11, 93042 Regensburg, Germany
Berit Lilje: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Nicolas Rapin: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Frederik Otzen Bagger: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Mette Jørgensen: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark
Peter Refsing Andersen: Centre for mRNP Biogenesis and Metabolism, C.F. Møllers Alle 3, Building 1130, DK-8000 Aarhus, Denmark
Nicolas Bertin: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Owen Rackham: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
A. Maxwell Burroughs: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
J. Kenneth Baillie: Roslin Institute, Edinburgh University, Easter Bush, Midlothian, Edinburgh EH25 9RG, UK
Yuri Ishizu: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Yuri Shimizu: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Erina Furuhata: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Shiori Maeda: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Yutaka Negishi: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Christopher J. Mungall: Lawrence Berkeley National Laboratory, 1 Cyclotron Road MS 64-121, Berkeley, California 94720, USA
Terrence F. Meehan: EMBL Outstation - Hinxton, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK
Timo Lassmann: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Masayoshi Itoh: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Hideya Kawaji: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Naoto Kondo: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Jun Kawai: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Andreas Lennartsson: Karolinska Institutet, Hälsovägen 7, SE-4183 Huddinge, Stockholm, Sweden
Carsten O. Daub: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Peter Heutink: VU University Medical Center, van der Boechorststraat 7, 1081 BT Amsterdam, Netherlands
David A. Hume: Roslin Institute, Edinburgh University, Easter Bush, Midlothian, Edinburgh EH25 9RG, UK
Torben Heick Jensen: Centre for mRNP Biogenesis and Metabolism, C.F. Møllers Alle 3, Building 1130, DK-8000 Aarhus, Denmark
Harukazu Suzuki: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Yoshihide Hayashizaki: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Ferenc Müller: School of Clinical and Experimental Medicine, College of Medical and Dental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
Alistair R. R. Forrest: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Piero Carninci: RIKEN OMICS Science Centre, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
Michael Rehli: University Hospital Regensburg, Franz-Josef-Strauss-Allee 11, 93042 Regensburg, Germany
Albin Sandelin: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark

Nature, 2014, vol. 507, issue 7493, 455-461

Abstract: Abstract Enhancers control the correct temporal and cell-type-specific activation of gene expression in multicellular eukaryotes. Knowing their properties, regulatory activity and targets is crucial to understand the regulation of differentiation and homeostasis. Here we use the FANTOM5 panel of samples, covering the majority of human tissues and cell types, to produce an atlas of active, in vivo-transcribed enhancers. We show that enhancers share properties with CpG-poor messenger RNA promoters but produce bidirectional, exosome-sensitive, relatively short unspliced RNAs, the generation of which is strongly related to enhancer activity. The atlas is used to compare regulatory programs between different cells at unprecedented depth, to identify disease-associated regulatory single nucleotide polymorphisms, and to classify cell-type-specific and ubiquitous enhancers. We further explore the utility of enhancer redundancy, which explains gene expression strength rather than expression patterns. The online FANTOM5 enhancer atlas represents a unique resource for studies on cell-type-specific enhancers and gene regulation.

Date: 2014
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DOI: 10.1038/nature12787

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